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Stephen M. Lenfest, Andreea Vaduva-Nemes and Michael S. Okun

In this paper the authors aim to review Dr. Henry Head's famous and dramatic nerve sectioning experiment. They discuss the implications of his experimental approach as well as the effect his experiment had on the field of neurology. Henry Head was a prominent British neurologist who contributed greatly to the understanding of the sensory examination through an experiment in which he had his own radial nerve transected. Head carefully documented the sensory changes following the sectioning. He hypothesized the existence of two separate sensory systems: protopathic and epicritic. Head was one of the first scientists to speculate on sensory dissociation, and his writings generated both enthusiasm and controversy. Although the ethical issue of self-experimentation was raised by his bold experiment and many aspects of his investigations and conclusions have been criticized, Head undoubtedly contributed important clinical lessons to neurology. Arguably, Henry Head's greatest contribution was the realization that the neurological portion of the sensory examination was anything but straightforward.

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Adam P. Burdick, Hubert H. Fernandez, Michael S. Okun, Yueh-Yun Chi, Charles Jacobson and Kelly D. Foote

Object

Adverse event (AE) rates for deep brain stimulation (DBS) are variable, due to various methodologies used for identifying, collecting, and reporting AEs. This lack of a prospective, standardized AE collection method is a shortcoming in the advancement of DBS. In this paper the authors disclose the standardized and prospectively recorded AE data from their institution, correlated with clinical outcome and quality of life (QOL) measures.

Methods

All patients who underwent operations at the authors' institution for Parkinson disease (PD), essential tremor, dystonia, other tremor, and obsessive-compulsive disorder were included. Complications occurring intraoperatively or within the first 180 days following surgery were recorded, analyzed, and classified as mild, moderate, or severe, regardless of their perceived relationship to the procedure. The presence, frequency, and severity of AEs were compared with the following outcome measurements: postoperative change in the QOL scales (Medical Outcomes Study 36-Item Short-Form Survey, 39-Item PD Questionnaire); motor scales (Tremor Rating Scale, Unified Dystonia Rating Scale, Unified PD Rating Scale); and Patient Global Impression Scale (PGIS).

Results

Two hundred seventy DBS procedures were performed in 198 patients. Three hundred AEs were recorded in 146 (54.1%) of the 270 procedures, and the AEs were recorded in 119 (60.1%) of 198 patients. Of the 198 patients, the maximum severity of AEs was mild in 28 (14.1%), moderate in 35 (17.7%), and severe in 56 (28.3%). Of the 300 AEs, 102 (34.1%) of 299 were mild, 106 (35.5%) were moderate, and 91 (30.4%) were severe. The AEs were classified as probably not stimulation induced in 10 (3.4%) of 297, probably in 44 (14.9%), unclear for 89 (30%), and not applicable to stimulation in 154 (51.9%). Adverse events were also classified as probably related to surgery in 111 (37.2%) of 298, possibly related in 96 (32.2%), and probably not related to surgery in 91 (30.5%). There was no significant difference (p = 0.22) in QOL outcomes among patients who had no AEs compared with those who experienced mild, moderate, or severe AEs. There was no significant difference in QOL outcomes between patients who did not experience an AE compared with those who experienced any AE. There was no significant difference in the mean General PGIS score between patients without an AE versus those with any AE, as well as on the Symptom-Specific PGIS. Motor function outcomes did not vary between patients with or without AEs. For patients with PD with or without AEs, there was no significant difference in preoperative off-medicine Unified PD Rating Scale score and postoperative 6-month on-medication/on-stimulation change scores (p = 0.59). For patients with tremor there were no differences between those with or without AEs on the Tremor Rating Scale for motor function or activities of daily living. Patients with dystonia with and without AEs showed no differences in the Unified Dystonia Rating Scale.

Conclusions

Prospectively and systematically recording AEs may result in higher AE rates, but this does not correlate with poorer QOL, motor function, or patient-oriented outcome scores.

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Takashi Morishita, Kelly D. Foote, Samuel S. Wu, Charles E. Jacobson IV, Ramon L. Rodriguez, Ihtsham U. Haq, Mustafa S. Siddiqui, Irene A. Malaty, Christopher J. Hass and Michael S. Okun

Object

Microelectrode recording (MER) and macrostimulation (test stimulation) are used to refine the optimal deep brain stimulation (DBS) lead placement within the operative setting. It is well known that there can be a microlesion effect with microelectrode trajectories and DBS insertion. The aim of this study was to determine the impact of intraoperative MER and lead placement on tremor severity in a cohort of patients with essential tremor.

Methods

Consecutive patients with essential tremor undergoing unilateral DBS (ventral intermediate nucleus stimulation) for medication-refractory tremor were evaluated. Tremor severity was measured at 5 time points utilizing a modified Tremor Rating Scale: 1) immediately before MER; 2) immediately after MER; 3) immediately after lead implantation; 4) 6 months after DBS implantation in the off-DBS condition; and 5) 6 months after implantation in the on-DBS condition. To investigate the impact of the MER and DBS lead placement, Wilcoxon signed-rank tests were applied to test changes in tremor severity scores over the surgical course. In addition, a generalized linear mixed model including factors that potentially influenced the impact of the microlesion was also used for analysis.

Results

Nineteen patients were evaluated. Improvement was noted in the total modified Tremor Rating Scale, postural, and action tremor scores (p < 0.05) as a result of MER and DBS lead placement. The improvements observed following lead placement were similar in magnitude to what was observed in the chronically programmed clinic setting parameters at 6 months after lead implantation. Improvement in tremor severity was maintained over time even in the off-DBS condition at 6 months, which was supportive of a prolonged microlesion effect. The number of macrostimulation passes, the number of MER passes, and disease duration were not related to the change in tremor severity score over time.

Conclusions

Immediate improvement in postural and intention tremors may result from MER and DBS lead placement in patients undergoing DBS for essential tremor. This improvement could be a predictor of successful DBS lead placement at 6 months. Clinicians rating patients in the operating room should be aware of these effects and should consider using rating scales before and after lead placement to take these effects into account when evaluating outcome in and out of the operating room.

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Editorial

Unilateral or bilateral deep brain stimulation

Kim J. Burchiel

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Maryam Rahman, Muhammad M. Abd-El-Barr, Vinata Vedam-Mai, Kelly D. Foote, Gregory J. A. Murad, Michael S. Okun and Steven N. Roper

Given the tremendous success of deep brain stimulation (DBS) for the treatment of movement and neuropsychiatric disorders, clinicians have begun to open up to the possible use of electrical stimulation for the treatment of patients with uncontrolled seizures. This process has resulted in the discovery of a wide array of DBS targets, including the cerebellum, hypothalamus, hippocampus, basal ganglia, and various thalamic nuclei. Despite the ambiguity of the mechanism of action and the unknowns surrounding potentially ideal stimulation settings, several recent trials have empirically demonstrated reasonable efficacy in selected cases of medication-refractory seizures. These exciting results have fueled a number of studies aimed at firmly establishing DBS as an effective treatment for selected cases of intractable epilepsy, and many companies are aiming at Food and Drug Administration approval. We endeavor to review the studies in the context of the various DBS targets and their relevant circuitry for epilepsy. Based on the unfolding research, DBS has the potential to play an important role in treating refractory epilepsy. The challenge, as in movement disorders, is to assemble interdisciplinary teams to screen, implant, and follow patients, and to clarify patient selection. The future will undoubtedly be filled with optimization of targets and stimulation parameters and the development of best practices. With tailored therapeutic approaches, epilepsy patients have the potential to improve with DBS.

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Takashi Tsuboi, Janine Lemos Melo Lobo Jofili Lopes, Kathryn Moore, Bhavana Patel, Joseph Legacy, Adrianna M. Ratajska, Dawn Bowers, Robert S. Eisinger, Leonardo Almeida, Kelly D. Foote, Michael S. Okun and Adolfo Ramirez-Zamora

OBJECTIVE

Few studies have reported long-term outcomes of globus pallidus internus (GPi) deep brain stimulation (DBS) in Parkinson’s disease (PD). The authors aimed to investigate long-term outcomes of bilateral GPi DBS for 5 years and beyond for PD patients.

METHODS

The authors retrospectively analyzed the clinical outcomes in 65 PD patients treated with bilateral GPi DBS at a single center. The outcome measures of motor symptoms and health-related quality of life (HRQoL) included the Unified Parkinson’s Disease Rating Scale (UPDRS) and the Parkinson’s Disease Questionnaire (PDQ-39). Scores at baseline were compared with those at 1, 3, 5, and 6–8 years after implantation using Wilcoxon signed-rank tests with α correction.

RESULTS

GPi DBS significantly improved the off-medication UPDRS III total scores, UPDRS IV, and dyskinesia score at 1 year when compared with baseline (all p < 0.001). The off- and on-medication tremor scores, UPDRS IV, and dyskinesia scores showed moderate and sustained improvement (the ranges of the mean percentage improvement at each time point were 61%–75%, 30%–80%, 29%–40%, and 40%–65%, respectively) despite lacking statistical significance at long-term follow-up with diminishing sample sizes. The off-medication UPDRS III total scores did not show significant improvement at 5 years or later, primarily because of worsening in rigidity, akinesia, speech, gait, and postural stability scores. The on-medication UPDRS III total scores also worsened over time, with a significant worsening at 6–8 years when compared with baseline (p = 0.008). The HRQoL analyses based on the PDQ-39 revealed significant improvement in the activities of daily living and discomfort domains at 1 year (p = 0.003 and 0.006, respectively); however, all the domains showed gradual worsening at the later time points without reaching statistical significance. At 3 years, the communication domain showed significant worsening compared with baseline scores (p = 0.002).

CONCLUSIONS

GPi DBS in PD patients in this single-center cohort was associated with sustained long-term benefits in the off- and on-medication tremor score and motor complications. HRQoL and the cardinal motor symptoms other than tremor may worsen gradually in the long term. When counseling patients, it is important to recognize that benefits in tremor and dyskinesia are expected to be most persistent following bilateral GPi DBS implantation.

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Genko Oyama, Michael S. Okun, Theresa A. Zesiewicz, Tiffany Tamse, Janet Romrell, Pamela Zeilman and Kelly D. Foote

Object

The purpose of this paper is to present 4 cases that illustrate the management and outcome of subdural hematoma (SDH) following deep brain stimulation (DBS) lead implantation.

Methods

The authors identified 4 cases of SDH following DBS lead implantation from a pool of 500 consecutive lead implantations (incidence 0.08%) performed at the University of Florida. Cases were characterized by chart review, serial Unified Parkinson's Disease Rating Scale evaluations, and changes on serial postoperative imaging studies.

Results

Two of the 4 patients with DBS-related SDH were clinically symptomatic. In the other 2 cases the SDH was incidentally discovered on routine postoperative lead localization imaging studies. None of the patients required craniotomy for evacuation of the SDH in the acute phase. Three of the 4 cases were managed with bur hole drainage in the chronic phase, and one was successfully managed nonoperatively. In all 4 cases, thresholds for stimulationinduced side effects were lower during initial postoperative programming than during intraoperative macrostimulation. Expected clinical improvement from DBS was achieved without lead revision in all 4 cases, but only after a significant delay.

Conclusions

Subdural hematoma is a rare and potentially avoidable complication of DBS that does not typically mandate acute hematoma evacuation or hardware revision and does not preclude an excellent outcome from DBS therapy. The clinical picture and apparent lead position tend to improve with time, and it may be wise to delay repositioning of an ineffective DBS lead following a hemorrhage until the DBS lead and surrounding brain tissue have settled into their final position and the insulted brain has had sufficient time to recover.

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Houtan A. Taba, Samuel S. Wu, Kelly D. Foote, Chris J. Hass, Hubert H. Fernandez, Irene A. Malaty, Ramon L. Rodriguez, Yunfeng Dai, Pamela R. Zeilman, Charles E. Jacobson IV and Michael S. Okun

Object

In this paper, the authors' aim was to examine reasons underpinning decisions to undergo, or alternatively forgo, a second-sided deep brain stimulation (DBS) implantation in patients with Parkinson disease (PD).

Methods

Fifty-two patients with Parkinson disease (PD) were randomized to receive DBS to the subthalamic nucleus or globus pallidus internus (GPi) as part of the COMPARE trial. Forty-four patients had complete data sets. All patients were offered a choice at 6 months after unilateral implantation whether to receive a contralateral DBS implant. All patients had advanced PD. The mean patient age was 59.8 years (range 43–76 years), and the mean duration of disease was 12.2 years (range 5–21 years). The mean baseline Unified Parkinson's Disease Rating Scale (UPDRS)–III motor score was 42.7. The main outcome measures used in this study were the UPDRS-III Motor Scale and the UPDRS-IV Dyskinesia Scale.

Results

Twenty-one (48%) of the 44 patients in the cohort did not undergo bilateral implantation and have been successfully treated for an average of 3.5 years; of these, 14 (67%) had a GPi target. The most common reason for adding a second side was inadequacy to address motor symptoms. Patient satisfaction with motor outcomes after unilateral DBS implantation was the most common reason for not undergoing bilateral implantation. Those who chose a second DBS procedure had significantly higher baseline UPDRS-III motor and ipsilateral UPDRS-III scores, and a significantly lower asymmetrical index. The logistic regression analysis revealed that the odds of proceeding to bilateral DBS was 5.2 times higher for STN than for GPi DBS. For every 1% increase in asymmetry, the odds of bilateral DBS decreased by 0.96.

Conclusions

Unilateral DBS is an effective treatment for a subset of patients with PD. Baseline asymmetry is an important factor in the effectiveness and decision-making process between unilateral and bilateral DBS. Patients with GPi DBS in this cohort were more likely to choose to remain with unilateral implantation.

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Rene Molina, Michael S. Okun, Jonathan B. Shute, Enrico Opri, P. Justin Rossi, Daniel Martinez-Ramirez, Kelly D. Foote and Aysegul Gunduz

Deep brain stimulation (DBS) has emerged as a promising intervention for the treatment of select movement and neuropsychiatric disorders. Current DBS therapies deliver electrical stimulation continuously and are not designed to adapt to a patient’s symptoms. Continuous DBS can lead to rapid battery depletion, which necessitates frequent surgery for battery replacement. Next-generation neurostimulation devices can monitor neural signals from implanted DBS leads, where stimulation can be delivered responsively, moving the field of neuromodulation away from continuous paradigms. To this end, the authors designed and chronically implemented a responsive stimulation paradigm in a patient with medically refractory Tourette syndrome. The patient underwent implantation of a responsive neurostimulator, which is capable of responsive DBS, with bilateral leads in the centromedian-parafascicular (Cm-Pf) region of the thalamus. A spectral feature in the 5- to 15-Hz band was identified as the control signal. Clinical data collected prior to and after 12 months of responsive therapy revealed improvements from baseline scores in both Modified Rush Tic Rating Scale and Yale Global Tic Severity Scale scores (64% and 48% improvement, respectively). The effectiveness of responsive stimulation (p = 0.16) was statistically identical to that of scheduled duty cycle stimulation (p = 0.33; 2-sided Wilcoxon unpaired rank-sum t-test). Overall, responsive stimulation resulted in a 63.3% improvement in the neurostimulator’s projected mean battery life. Herein, to their knowledge, the authors present the first proof of concept for responsive stimulation in a patient with Tourette syndrome.